Arabidopsis phospholipase Dδ is involved in basal defense and nonhost resistance to powdery mildew fungi

Plant Physiology

Volumn 163, Issue 2, 2013, Pages 896-906

  Pinosa, Francesco ^a   Buhot, Nathalie ^a   Kwaaitaal, Mark ^b   Fahlberg, Per ^a   Thordal Christensen, Hans ^b   Ellerström, Mats ^a   Andersson, Mats X ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; BLUMERIA GRAMINIS F. SP. HORDEI; ERYSIPHALES; ERYSIPHE PISI; FUNGI; HORDEUM; PISUM SATIVUM;

ARABIDOPSIS PROTEIN; CHITIN; ISOENZYME; MESSENGER RNA; PATTERN RECOGNITION RECEPTOR; PHOSPHATIDIC ACID; PHOSPHOLIPASE D; PHOSPHOLIPASE D DELTA;

ARABIDOPSIS; ARTICLE; ASCOMYCETES; CELL MEMBRANE; DISEASE RESISTANCE; DRUG EFFECT; ENZYMOLOGY; FUNGUS SPORE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PEA; PHYSIOLOGY; PLANT DISEASE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; ASCOMYCOTA; CELL MEMBRANE; CHITIN; DISEASE RESISTANCE; GENE EXPRESSION REGULATION, PLANT; ISOENZYMES; PEAS; PHOSPHATIDIC ACIDS; PHOSPHOLIPASE D; PLANT DISEASES; RECEPTORS, PATTERN RECOGNITION; RNA, MESSENGER; SPORES, FUNGAL;

EID: 84885223321     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.223503     Document Type: Article

References (65)

1. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657
2. Andersson MX, Kourtchenko O, Dangl JL, Mackey D, Ellerström M (2006) Phospholipase-dependent signalling during the AvrRpm1and AvrRpt2-induced disease resistance responses in Arabidopsis thaliana. Plant J 47: 947-959
3. Assaad FF, Qiu J-L, Youngs H, Ehrhardt D, Zimmerli L, Kalde M, Wanner G, Peck SC, Edwards H, Ramonell K, et al (2004) The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. Mol Biol Cell 15: 5118-5129
4. Bargmann BOR, Munnik T (2006) The role of phospholipase D in plant stress responses. Curr Opin Plant Biol 9: 515-522
5. Bednarek P, Pislewska-Bednarek M, Svatos A, Schneider B, Doubsky J, Mansurova M, Humphry M, Consonni C, Panstruga R, Sanchez-Vallet A, et al (2009) A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323: 101-106
6. Bhat RA, Miklis M, Schmelzer E, Schulze-Lefert P, Panstruga R (2005) Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain. Proc Natl Acad Sci USA 102: 3135-3140
7. Böhlenius H, Mørch SM, Godfrey D, Nielsen ME, Thordal-Christensen H (2010) The multivesicular body-localized GTPase ARFA1b/1c is important for callose deposition and ROR2 syntaxin-dependent preinvasive basal defense in barley. Plant Cell 22: 3831-3844
8. Boller T, Felix G (2009) A renaissance of elicitors: perception of microbeassociated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60: 379-406
9. 2+ sensor protein kinases. Nature 464: 418-422
10. Camehl I, Drzewiecki C, Vadassery J, Shahollari B, Sherameti I, Forzani C, Munnik T, Hirt H, Oelmüller R (2011) The OXI1 kinase pathway mediates Piriformospora indica-induced growth promotion in Arabidopsis. PLoS Pathog 7: e1002051
11. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacteriummediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
12. Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, Qiu J-L, Hückelhoven R, Stein M, Freialdenhoven A, Somerville SC, et al (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425: 973-977
13. de Jong CF, Laxalt AM, Bargmann BOR, de Wit PJGM, Joosten MHAJ, Munnik T (2004) Phosphatidic acid accumulation is an early response in the Cf-4/Avr4 interaction. Plant J 39: 1-12
14. Guo L, Devaiah SP, Narasimhan R, Pan X, Zhang Y, Zhang W, Wang X (2012) Cytosolic glyceraldehyde-3-phosphate dehydrogenases interact with phospholipase Dd to transduce hydrogen peroxide signals in the Arabidopsis response to stress. Plant Cell 24: 2200-2212
15. Hardham AR, Jones DA, Takemoto D (2007) Cytoskeleton and cell wall function in penetration resistance. Curr Opin Plant Biol 10: 342-348
16. Hong Y, Pan X, Welti R, Wang X (2008) Phospholipase Da3 is involved in the hyperosmotic response in Arabidopsis. Plant Cell 20: 803-816
17. Hückelhoven R (2007) Cell wall-associated mechanisms of disease resistance and susceptibility. Annu Rev Phytopathol 45: 101-127
18. Jenkins GM, Frohman MA (2005) Phospholipase D: a lipid centric review. Cell Mol Life Sci 62: 2305-2316
19. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444: 323-329
20. Kachroo A, Kachroo P (2009) Fatty acid-derived signals in plant defense. Annu Rev Phytopathol 47: 153-176
21. Karimi M, De Meyer B, Hilson P (2005) Modular cloning in plant cells. Trends Plant Sci 10: 103-105
22. Kirik A, Mudgett MB (2009) SOBER1 phospholipase activity suppresses phosphatidic acid accumulation and plant immunity in response to bacterial effector AvrBsT. Proc Natl Acad Sci USA 106: 20532-20537
23. Kirsch C, Takamiya-Wik M, Reinold S, Hahlbrock K, Somssich IE (1997) Rapid, transient, and highly localized induction of plastidial v-3 fatty acid desaturase mRNA at fungal infection sites in Petroselinum crispum. Proc Natl Acad Sci USA 94: 2079-2084
24. Kleinboelting N, Huep G, Kloetgen A, Viehoever P, Weisshaar B (2012) GABI-Kat SimpleSearch: new features of the Arabidopsis thaliana T-DNA mutant database. Nucleic Acids Res 40: D1211-D1215
25. Koch E, Slusarenko A (1990) Arabidopsis is susceptible to infection by a downy mildew fungus. Plant Cell 2: 437-445
26. Kwaaitaal M, Huisman R, Maintz J, Reinstädler A, Panstruga R (2011) Ionotropic glutamate receptor (iGluR)-like channels mediate MAMPinduced calcium influx in Arabidopsis thaliana. Biochem J 440: 355-365
27. Laxalt AM, Munnik T (2002) Phospholipid signalling in plant defence. Curr Opin Plant Biol 5: 332-338
28. Lerchner A, Mansfeld J, Kuppe K, Ulbrich-Hofmann R (2006) Probing conserved amino acids in phospholipase D (Brassica oleracea var. capitata) for their importance in hydrolysis and transphosphatidylation activity. Protein Eng Des Sel 19: 443-452
29. Li M, Hong Y, Wang X (2009) Phospholipase Dand phosphatidic acidmediated signaling in plants. Biochim Biophys Acta 1791: 927-935
30. Li M, Qin C, Welti R, Wang X (2006) Double knockouts of phospholipases Dz1 and Dz2 in Arabidopsis affect root elongation during phosphate-limited growth but do not affect root hair patterning. Plant Physiol 140: 761-770
31. Li W, Li M, Zhang W, Welti R, Wang X (2004) The plasma membranebound phospholipase Ddelta enhances freezing tolerance in Arabidopsis thaliana. Nat Biotechnol 22: 427-433
32. Lipka U, Fuchs R, Lipka V (2008) Arabidopsis non-host resistance to powdery mildews. Curr Opin Plant Biol 11: 404-411
33. Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M, Stein M, Landtag J, Brandt W, Rosahl S, Scheel D, et al (2005) Preand postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310: 1180-1183
34. Ma W, Berkowitz GA (2007) The grateful dead: calcium and cell death in plant innate immunity. Cell Microbiol 9: 2571-2585
35. 2+, cAMP, and transduction of non-self perception during plant immune responses. Proc Natl Acad Sci USA 106: 20995-21000
36. Meyer D, Pajonk S, Micali C, O'Connell R, Schulze-Lefert P (2009) Extracellular transport and integration of plant secretory proteins into pathogen-induced cell wall compartments. Plant J 57: 986-999
37. Micali C, Göllner K, Humphry M, Consonni C, Panstruga R (2008) The powdery mildew disease of Arabidopsis: a paradigm for the interaction between plants and biotrophic fungi. The Arabidopsis Book 6: e0115, doi/10.1199/tab.0115
38. Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H, Shibuya N (2007) CERK1, a LysM receptorkinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci USA 104: 19613-19618
39. Monaghan J, Zipfel C (2012) Plant pattern recognition receptor complexes at the plasma membrane. Curr Opin Plant Biol 15: 349-357
40. Munnik T, Arisz SA, De Vrije T, Musgrave A (1995) G protein activation stimulates phospholipase D signaling in plants. Plant Cell 7: 2197-2210
41. Nielsen ME, Feechan A, Böhlenius H, Ueda T, Thordal-Christensen H (2012) Arabidopsis ARF-GTP exchange factor, GNOM, mediates transport required for innate immunity and focal accumulation of syntaxin PEN1. Proc Natl Acad Sci USA 109: 11443-11448
42. 2+ and phosphorylation. J Biol Chem 283: 8885-8892
43. 2+ and phosphatidylinositol 4,5-biphosphate. J Biol Chem 277: 49685-49690
44. Qin C, Wang X (2002) The Arabidopsis phospholipase D family: characterization of a calcium-independent and phosphatidylcholine-selective PLDz1 with distinct regulatory domains. Plant Physiol 128: 1057-1068
45. Raho N, Ramirez L, Lanteri ML, Gonorazky G, Lamattina L, ten Have A, Laxalt AM (2011) Phosphatidic acid production in chitosan-elicited tomato cells, via both phospholipase D and phospholipase C/diacylglycerol kinase, requires nitric oxide. J Plant Physiol 168: 534-539
46. Ron M, Avni A (2004) The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell 16: 1604-1615
47. Scholl RL, May ST, Ware DH (2000) Seed and molecular resources for Arabidopsis. Plant Physiol 124: 1477-1480
48. Schulze-Lefert P, Panstruga R (2011) A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends Plant Sci 16: 117-125
49. Schwessinger B, Zipfel C (2008) News from the frontline: recent insights into PAMP-triggered immunity in plants. Curr Opin Plant Biol 11: 389-395
50. Shimizu T, Nakano T, Takamizawa D, Desaki Y, Ishii-Minami N, Nishizawa Y, Minami E, Okada K, Yamane H, Kaku H, et al (2010) Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J 64: 204-214
51. Stein M, Dittgen J, Sánchez-Rodríguez C, Hou B-H, Molina A, Schulze-Lefert P, Lipka V, Somerville S (2006) Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18: 731-746
52. Suzuki K, Yano A, Nishiuchi T, Nakano T, Kodama H, Yamaguchi K, Shinshi H (2007) Comprehensive analysis of early response genes to two different microbial elicitors in tobacco cells. Plant Sci 173: 291-301
53. Testerink C, Munnik T (2011) Molecular, cellular, and physiological responses to phosphatidic acid formation in plants. J Exp Bot 62: 2349-2361
54. Thordal-Christensen H (2003) Fresh insights into processes of nonhost resistance. Curr Opin Plant Biol 6: 351-357
55. Torres MA, Jones JDG, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141: 373-378
56. van der Luit AH, Piatti T, van Doorn A, Musgrave A, Felix G, Boller T, Munnik T (2000) Elicitation of suspension-cultured tomato cells triggers the formation of phosphatidic acid and diacylglycerol pyrophosphate. Plant Physiol 123: 1507-1516
57. Wan J, Zhang XC, Neece D, Ramonell KM, Clough S, Kim SY, Stacey MG, Stacey G (2008) A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20: 471-481
58. Wang C, Wang X (2001) A novel phospholipase D of Arabidopsis that is activated by oleic acid and associated with the plasma membrane. Plant Physiol 127: 1102-1112
59. Wang X (2004) Lipid signaling. Curr Opin Plant Biol 7: 329-336
60. Yamaguchi T, Minami E, Ueki J, Shibuya N (2005) Elicitor-induced activation of phospholipases plays an important role for the induction of defense responses in suspension-cultured rice cells. Plant Cell Physiol 46: 579-587
61. Young SA, Wang X, Leach JE (1996) Changes in the plasma membrane distribution of rice phospholipase D during resistant interactions with Xanthomonas oryzae pv oryzae. Plant Cell 8: 1079-1090
62. Zhang W, Qin C, Zhao J, Wang X (2004) Phospholipase Da1-derived phosphatidic acid interacts with ABI1 phosphatase 2C and regulates abscisic acid signaling. Proc Natl Acad Sci USA 101: 9508-9513
63. Zhang W, Wang C, Qin C, Wood T, Olafsdottir G, Welti R, Wang X (2003) The oleate-stimulated phospholipase D, PLDδ, and phosphatidic acid decrease H2O2-induced cell death in Arabidopsis. Plant Cell 15: 2285-2295
64. Zhang Z, Lenk A, Andersson MX, Gjetting T, Pedersen C, Nielsen ME, Newman M-A, Hou B-H, Somerville SC, Thordal-Christensen H (2008) A lesion-mimic syntaxin double mutant in Arabidopsis reveals novel complexity of pathogen defense signaling. Mol Plant 1: 510-527
65. Zimmerli L, Stein M, Lipka V, Schulze-Lefert P, Somerville S (2004) Host and non-host pathogens elicit different jasmonate/ethylene responses in Arabidopsis. Plant J 40: 633-646